Multiparasitism in gills of Metynnis lippincottianus from the environmental
protection area of Curiaú river, Eastern Amazon
Multiparasitismo em brânquias de Metynnis lippincottianus da área
de proteção ambiental do rio Curiaú, Amazônia Oriental
Abthyllane Amaral de Carvalho
1Roger Leomar da Silva Ferreira
1Priscila Gomes de Araújo
1Márcio Charles da Silva Negrão
2Marcela Nunes Videira
3*ISSNe 1678-4596
INTRODUCTION
The high ichthyological diversity of
Amazon has been a subject of study for researchers
(TAVARES et al., 2018; DE ANDRADE et al., 2018;
ZATTI et al., 2018; BITTENCOURT et al., 2014),
but still many issues are need to be studied and
understood. (MOREIRA et al., 2010). This geographic
area also encompasses ecosystems that are vital for
maintaining the surrounding environment, such as
floodplain forests (BATISTA et al., 2015). In the state
of Amapá, floodplain forests are the second largest
ecosystem in the state, occupy 4.8% of the territory
while the rainforest occupies approximately 70% of
the state of the Amapá. Since this area is a suitable
habitat for many native species (QUEIROZ et al,
1Laboratório de Morfofisiologia e Sanidade Animal, Programa de Pós-graduação em Ciências Ambientais, Universidade Federal do Amapá
(UNIFAP), Macapá, AP, Brasil.
2Laboratório de Morfofisiologia de Sanidade Animal, Programa de Pós-graduação em Biodiversidade Tropical, Universidade Federal do
Amapá (UNIFAP), Macapá, AP, Brasil.
3Laboratório de Morfofisiologia de Sanidade Animal, Programa de Pós-graduação em Ciências Ambientais, Universidade do Estado do Amapá
(UEAP), Campus I, 68900-070, Macapá, AP, Brasil. E-mail: marcela.videira@ueap.edu.br. *Corresponding author.
ABSTRACT: The high fish diversity of the Amazon has been the subject of study for several research projects because of the importance
of its ecosystems. The Environmental Protection Area of the Curiaú River is composed of permanent and temporary lakes within the floodplain forests, favoring a rich diversity of fish species. Pratinha. (Metynnis lippincottianus) is an ornamental fish, widely distributed throughout Brazil and French Guiana. Fish parasites may reflect the environmental quality, as well as the habits of their host. Considering the importance of understanding and contributing to the expansion of studies on fish parasites, the present study aimed to investigate the gills of Metynnis lippincottianus from the Curiaú River basin in the municipality of Macapá (Eastern Amazon). A total of 200 specimens of Metynnis lippincottianus from the Curiaú River were examined and 89% of the analyzed fish were parasitized by metacercariae, Dactylogyridae gen. sp., Piscinoodinium pillulare, Trichodina sp., Henneguya sp., and Myxobolus sp. Despite this high parasitic load, body conditions were not affected. This is the first documented incidence of a species belonging to the Phylum Cnidaria: Myxozoa in Metynnis lippincottianus.
Key words: ornamental fish, parasitic fauna, infection.
RESUMO: A alta diversidade ictiológica da Amazônia tem sido fonte de estudo de diversas pesquisas, por esta região amazônica englobar
alguns ecossistemas importantes. A Área de Proteção Ambiental do Rio Curiaú é composta por lagos permanentes e temporários dentro das florestas de várzeas, o que favorece em uma rica diversidade de espécies de peixes. Metynnis lippincottianus é um peixe ornamental, amplamente distribuído pelo Brasil e Guiana Francesa. Os parasitos de peixes podem refletir a qualidade ambiental, assim como nos hábitos de seu hospedeiro. Considerando a importância de entender e contribuir para a expansão dos estudos sobre parasitos de peixes, o presente estudo teve como objetivo, investigar as brânquias de Metynnis lippincottianus oriundos da bacia do Rio Curiaú no município de Macapá-AP (Amazônia Oriental). Foram examinados 200 exemplares de Metynnis lippincottianus, oriundos do rio Curiaú, sendo que 89% dos peixes analisados estavam parasitados por parasitos diversos: Piscinoodinium pillulare, Trichodina sp., Henneguya sp., Myxobolus sp., monogenoide da família Dactylogyridae e metacercárias. Apesar dessa alta carga parasitária, as condições corporais não foram afetadas. Esta é a primeira ocorrência de espécies do filo Cnidaria: Myxozoa em Metynnis lippincottianus.
Palavras- chave: peixe ornamental, parasitofauna, infecção.
2 Carvalho et al.
2013; PINTO, 2016), 20.83% of these floodplain
forest (4,632.71 hectares) are designated as the
Environmental Protection Area (APA) of the Curiaú
River (LIMA et al., 2013).
The APA of the Curiaú River is composed
of permanent and temporary lakes within the
floodplain forests, favoring a rich diversity of fish
species, such as Serrasalmus rhombeus (piranha),
Hoplosternum littorale (tamoatá), Cichla temensis
(tucunaré), Hoplias malabaricus (traíra), and
Piaractus mesopotamicus (pacu). Among these,
a species of ornamental importance, Metynnis
lippincottianus (Serrasalmidae) known popularly as
Pratinha is widely distributed in the Brazilian basins
and some French Guiana rivers. It has a diet based on
vegetables, seeds, phytoplankton, mollusks and some
arthropods and detritus (MOREIRA et al., 2009;
HOSHINO et al., 2014).
In the Amazon, several factors influence
the parasitic load of fish, such as seasonality, abiotic
and biotic factors in aquatic environment water, and
host ecology (NEVES et al., 2013). The diversity and
ecological function of the parasites in an ecosystem
can be used as tools for a better understanding of
the biosphere, as well as the parasitic indexes
that support parasite-host relationship analysis
(TAVARES-DIAS et al. 2014 CARDOSO et al.,
2018). TAKEMOTO et al. (2004) stated that all
fish hosted at least one species of parasite and the
location of the parasites may vary, where no organ is
free from parasitism, but one organ may have more
parasites than another organ.
Multiple studies have reported that gills
are one of the most parasitized organs (CARDOSO
et al., 2018; JERÔNIMO et al., 2014, GONÇALVES
et al., 2014, VENTURA et al., 2013, SANTOS et
al. 2013; OLIVEIRA et al., 2016). Gills are easily
damaged by parasitic infections, being the first
organ in contact with the external environment.
Additionally, gills perform several functions, such
as respiration, osmoregulation, and excretion. Gills
are an indicator of the rate of parasitism, based
on histopathological changes, such as respiratory
disorders and electrolyte imbalance
(FLORES-LOPES et al., 2011; NASCIMENTO et al., 2012).
Fish parasites may reflect the environmental
quality, as well as habits of their host, considering
the importance of understanding and contributing
to the expansion of studies on fish parasites
(FALKENBERG et al., 2019). Therefore, the present
study aimed to investigate the gills of Metynnis
lippincottianus from the Curiaú River basin in
Macapá (eastern Amazon).
MATERIALS AND METHODS
Study area
The Curiaú river basin measures
approximately 584.47 km
2, almost 40% of the Curiaú
River’s Environmental Protection Area (APA) (LIMA
et al., 2013). The Curiaú River’s mouth in the Amazon
River presents meandric characteristics, which may
be due to the greater turbulence in the river, caused
by the speed of the water current and the Amazonian
river tidal regime (VASCONCELOS et al., 2011).
Specimens of M. lippincottianus (COPE,
1870), common fish species of the Curiaú River (Point
1: 51º2’57,205” W 0º8’29” N; Point 2:51º2’30”,743
W 0º8’43,087” N), were collected during a 12-month
period, from August 2017 to August 2018. Collections
were carried out twice per month for parasitological
analysis, using a 20 mm net between knots measuring
five meters long and two meters high, being placed
in points with intense activity of fishing by the local
population (Figure 1).
Parasites sampling procedures
All fish were transported alive in vats
containing water from the environment and artificial
aeration, to the Laboratory of Morphophysiology
and Animal Health (LABMORSA) at the State
University of Amapá (UEAP). The specimens were
desensitized through a medullary incision, using
pincers and a scalpel. Then, biometric data such as
total length (cm), standard length (cm) and weight
(g) were measured.
The entire external surface, mouth, nostrils,
fins, and gills were analyzed using stereoscopic
binocular microscopes, to verify the existence of
parasites, cysts, or lesions. During the necropsy,
small gills fragments were separated between slides
and coverslips, wherein foci of parasite development
were identified via light microscope analysis.
Prevalence was used to analyze the
infection level of the parasites following the
recommendations of BUSH et al. (1997). A relative
condition factor for the host was determined using
body weight (g) and total length (cm) data following
LECREN (1951) where the expected and observed
weight are used to calculate, which has a value equal
to one (Kn=1) under normal conditions.
The project was submitted to the Ethics
Committee for Animal Use (CEUA), nº 012-CEUA/
CPAFAP and to the System of Authorization and
Information on Biodiversity (SISBIO) nº 50376-1.
A license was also obtained from the Secretary of
the Environment of the State of Amapá (SEMA-AP)
(letter nº 1014 / 2016), due to the status of the research
site as an Environmental Protection Area.
RESULTS AND DISCUSSION
The 200
specimens of M. lippincottianus
examined from the Curiaú River, had a mean total
length of 7.77±0.78 cm; standard mean length of
6.21±0.64 cm; and mean weight of 9.17±2.82 g.
Eighty-nine percent were parasitized by one or
more species. Three taxa (Ciliophora, Cnidaria
and Platyhelminthes) and 6 groups of parasites:
Piscinoodinium pillulare, Trichodina sp., Henneguya
sp., Myxobolus sp., monogenoids from the family
Dactylogyridae, and unidentified digenetics
(metacercariae) (Figure 2). Cnidarian Henneguya sp
.
presented the highest prevalence (89%) among the
parasites reported in gills; metacercariae showed the
lowest prevalence (15%).
The
dinoflagellata
Piscinoodinium
pillulare was found in the gills of 44% of the
analyzed M. lippincottianus specimens, which was
lower than the prevalence reported by FLORINDO
et al. (2017) in ornamental fish from Santa Catarina,
which was 75% in all fish. This same parasite
was reported in Cichlasoma amazonarum and in
Hemibrycon surinamensis of the Igarapé of Fortaleza
basin, Macapá, with a prevalence of 49% and 17.2%,
respectively (CARVALHO et al., 2017; HOSHINO
et al. 2014; HOSHINO et al., 2014). Piscinoodinium
pillulare is common in cold season of the year and is
responsible for outbreaks in aquaculture, which may
cause discomfort and a
sphyxia in hosts, as described
by SANT’ANA et al (2012).
Parasitic infection of the gills in the
genus Trichodina is the main cause of mortality
among fish farms (MACIEL et al., 2018). In this
study, the prevalence of Trichodina sp. in the gills
was 19%, which was higher than the prevalence
(10.4%) reported by NEVES et al. (2013) in
Astronotus ocelatus from Pracuúba Lake, Amapá.
Trichodina spp. was found in gills of Carnegiella
strigata, Carnegiella martae, and Nannostomus
eques, with a prevalence of 14.3%, 7.9%, and 9.7%,
respectively; all of these fish were collected from
the middle Rio Negro (TAVARES-DIAS et al.,
Figure 1 - Collection sites of Metynnis lippincottianus in the Curiaú River, eastern Amazonia (Brazil). Author: Cardoso-Junior, F. S.
4 Carvalho et al.
2010). Trichodina nobilis parasitized the gills in
64.3% and 84.2%, respectively, of in Pterophyllum
scalare and Mesonauta acora individuals (FARIAS
PANTOJA et al., 2015).
In the present study, the parasite that
presented the highest prevalence of infection
was Henneguya sp., which infected 89% of the
specimens analyzed. This prevalence was greater
than thatported re in Hypophthalmus marginatus of
the municipality of Cametá, in the state of Pará, in
which 80% of the individuals were parasitized by
Henneguya sp
. (VELASCO et al., 2015), this higher
prevalence can be related directly as the feeding
habit of the fish species, as well as the behavioral,
biological and physiological differences of these
fish (ISAAC et al., 2004) because these factors
can affect the structure of the parasite community
(CARVALHO et al., 2017). Henneguya sp. was also
described in Pimelodus maculatus, infecting 13.4%
of the gills (MARTINS et al., 2018). Henneguya
paraensis was reported in 60% of the gills of Cichla
temensis specimens studied (VELASCO et al., 2016).
Henneguya aequidens occurred in 33.3% of the gills
of Aequidens plagiozonatus individuals (VIDEIRA et
al., 2015); whereas in Arapaima gigas, Henneguya
arapaima parasitized the gill arches and gall bladder
with a prevalence of 11.7% and 82.3%, respectively
(FEIJÓ et al., 2008). This parasite has high specificity
for its host fish, and its parasitic action brings not only
ultrastructural damages that can result in death, but
also cause sterility of the host when housed in the
gonads and testicles (MATOS et al., 2001).
Myxobolus spp
. parasitized 65% of
gills of the fish examined, a value higher than that
reported in the heart of Pimelodus ornatus, from
the Arari Waterfall, which had a prevalence of
13.9% in the 43 specimens analyzed (MATOS et al.,
2014). LACERDA et al (2013) explained that the
discrimination of the fish parasitic fauna can be based
on premise that the different biogeographic regions
showed a range of possibilities for the parasitic fauna
structure in the host, thus explaining the differences
in parasites prevalence in their hosts. A species of
Myxobolus, Myxobolus maculatus, was found to
parasitize 40% of the kidneys of Metynnis maculatus,
a fish of the same genus as those researched in
this study, collected in the Amazon River estuary
(CASAL et al., 2002). Myxobolus insignis infected
the gills of 66.6% of Semaprochilodus insignis
(EIRAS et al., 2005) and Myxobolus sp. of 5.5% of
Colossoma macropomum (MACIEL et al., 2011),
both fish species being from the Amazon basin.
Myxobolus marajoensis, was found to parasitize the
intestinal musculature of 20% of fish from Paracauri
River, in the Island of Marajó-PA, Rhamdia quelen
(ABRUNHOSA et al., 2017).
Monogenoids of the family Dactylogyridae
presented the second highest prevalence, at 81.5% of
Figure 2 - Prevalence of the parasites present in the gills of Metynnis lippincottianus from Curiaú River, Eastern Amazon.
the specimens examined. HOSHINO &
TAVARES-DIAS (2014) described the presence of a species of
the family Dactylogyridae in M. lippincottianus of
the Igarapé Fortaleza basin / AP. The species reported
was Anacanthorus jegui, with a prevalence of 95%
in the 80 specimens analyzed. In another study,
conducted by REVERTER et al. (2016) in gills of
butterflies fishes of the Tropical Islands of the Western
Pacific, parasitism by monogenea communities of the
Dactylogyridae family to occurred with prevalences
between 40% and 100% in the analyzed species;
members of the family Dactylogyridae are thus
present in both freshwater and marine environments.
According to MENDOZA-FRANCO et al. (2018), the
occurrence of monogenea in ornamental freshwater
fish is due to the introduction of exotic fish that
harbor these parasites and the pollution of the natural
environment.
The presence of digenetic metacercariae
larvae in the gills of M. lippincottianus was observed
with the lowest prevalence among the parasites
reported — only 15% of the individuals examined were
infected. It was not possible to identify the individual
species of metacercariae. In studies conducted in
Lago Guaíba / RS, 13 species belonging to the phylum
Platyhelminthes were parasitizing the intestines,
gills, and stomach of Megaleporinus obtusidens,
with prevalence between 1.66% and 86.66% in
the 60 specimens analyzed (WENDT et al., 2018).
There were metacercariae of Posthodiplostomum
sp. parasitizing the gills of Auchenipterus nuchalis
(TAVARES-DIAS, 2017) and metacercariae in the
gills of 77.5% of M. lippincottianus (HOSHINO et
al., 2014); both fish species distributed the Igarapé
of Fortaleza basin. MORAIS et al., (2011) reported
metacercariae of Clinostomun marginatum and
Austrodiplostomum compactum, parasitizing 100%
and 15%, respectively, present in Pygocentrus
nattereri of central Amazon.
The relative factor of the host
(Kn=1.000±0.08) was not affected by the parasitism,
since it remained very close to the standard value,
that is Kn=1.0, according LECREN (1951), thus
indicating that the specimens’ condition was not
impacted, despite the high parasitic load. This
relative condition factor indicated the well-being
of the fish, thus measuring the state of animal
health (VAZZOLER, 1996, LIZAMA et al., 2006).
FALKENBERG et al. (2019) said that under natural
conditions, fish can be infected by many species,
which coexist and show interrelations, demonstrating
that each host has its own community of parasites and
that hosts acquire resistance, as well as adapt with the
presence of parasites and thus not have a negative
influence on the condition factor.
CONCLUSION
The parasitic fauna of the gills of M.
lippincottianus comprised micro and macroparasites,
was diverse in its composition, and was dominated
by the phylum Cnidaria: Myxozoa. Henneguya sp
.
was the most prevalent parasite, while metacercariae
were the least prevalent. The presence of protozoa,
Trichodina sp. and Piscinoodinium pillulare,
occurred in almost 50% of the specimens, and these
are primarily responsible for production losses in
aquaculture. The presence of two species of the genus
Myxobolus was observed, which were differentiated
based on spores of different shapes, since species
identification for myxozoa requires molecular
and ultrastructural analysis. This is first observed
occurrence of species belonging to the phylum
Cnidaria: Myxozoa in M. lippincottianus.
DECLARATION OF CONFLICT OF
INTERESTS
The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.
BIOETHICS AND BIOSSECURITY
COMMITTEE APPROVAL
This research was approved by the Animal Use Ethics Committee (CEUA) of EMBRAPA-AP, number 012-CEUA/CPAFAP and registered in the System of Authorization and Information of Biodiversity (SISBIO), nº 50376-1, as well as authorized by the Secretary of Environment of the State of Amapá (SEMA), for the reason of the study being conducted in Environmental Protection Area, under the official number 1014/2016.
AUTHORS’ CONTRIBUTIONS
All authors contributed equally for the conception and writing of the manuscript. All authors critically revised the manuscript and approved of the final version.
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